Identification of the First Gene Transfer Agent (GTA) Small Terminase in Rhodobacter capsulatus and Its Role in GTA Production and Packaging of DNA

J Virol. 2019 Nov 13;93(23):e01328-19. doi: 10.1128/JVI.01328-19. Print 2019 Dec 1.

Abstract

Genetic exchange mediated by viruses of bacteria (bacteriophages) is the primary driver of rapid bacterial evolution. The priority of viruses is usually to propagate themselves. Most bacteriophages use the small terminase protein to identify their own genome and direct its inclusion into phage capsids. Gene transfer agents (GTAs) are descended from bacteriophages, but they instead package fragments of the entire bacterial genome without preference for their own genes. GTAs do not selectively target specific DNA, and no GTA small terminases are known. Here, we identified the small terminase from the model Rhodobacter capsulatus GTA, which then allowed prediction of analogues in other species. We examined the role of the small terminase in GTA production and propose a structural basis for random DNA packaging.IMPORTANCE Random transfer of any and all genes between bacteria could be influential in the spread of virulence or antimicrobial resistance genes. Discovery of the true prevalence of GTAs in sequenced genomes is hampered by their apparent similarity to bacteriophages. Our data allowed the prediction of small terminases in diverse GTA producer species, and defining the characteristics of a "GTA-type" terminase could be an important step toward novel GTA identification. Importantly, the GTA small terminase shares many features with its phage counterpart. We propose that the GTA terminase complex could become a streamlined model system to answer fundamental questions about double-stranded DNA (dsDNA) packaging by viruses that have not been forthcoming to date.

Keywords: DNA packaging; DNA-binding proteins; Rhodobacter; antibiotic resistance; antimicrobial resistance; bacterial evolution; bacteriophage; bacteriophage assembly; gene transfer; gene transfer agent; horizontal gene transfer; terminase; transduction; virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteriophages / genetics
  • Capsid Proteins / genetics
  • DNA
  • DNA Packaging*
  • DNA-Binding Proteins
  • Drug Resistance, Bacterial
  • Endodeoxyribonucleases / genetics*
  • Endodeoxyribonucleases / metabolism
  • Evolution, Molecular
  • Gene Transfer, Horizontal*
  • Multigene Family
  • Rhodobacter capsulatus / genetics*
  • Rhodobacter capsulatus / virology
  • Sequence Alignment
  • Sequence Analysis, Protein
  • Transduction, Genetic
  • Virus Assembly

Substances

  • Capsid Proteins
  • DNA-Binding Proteins
  • DNA
  • Endodeoxyribonucleases
  • terminase